Inhibition of post-synaptic Kv7/KCNQ/M channels facilitates long-term potentiation in the hippocampus

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Petrovic, Milos M ^a,b   Nowacki, Jakub ^a   Olivo, Valeria ^a   Tsaneva Atanasova, Krasimira ^a   Randall, Andrew D ^a   Mellor, Jack R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

[No Author keywords available]

Indexed keywords

10,10 BIS(4 PYRIDINYLMETHYL) 9(10H) ANTHRACENONE; ADENOSINE DIPHOSPHATE; MUSCARINIC M1 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POTASSIUM CHANNEL KCNQ; CALCIUM; MUSCARINIC RECEPTOR; POTASSIUM CHANNEL KCNQ1;

ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; DEPOLARIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; NONHUMAN; PATCH CLAMP; POTASSIUM CONDUCTANCE; RAT; SYNAPSE; ACTION POTENTIAL; ANIMAL; DRUG ANTAGONISM; METABOLISM; PHYSIOLOGY;

RATTUS;

ACTION POTENTIALS; ANIMALS; CALCIUM; HIPPOCAMPUS; KCNQ1 POTASSIUM CHANNEL; LONG-TERM POTENTIATION; RATS; RECEPTORS, MUSCARINIC; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84856862144     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030402     Document Type: Article

References (56)

1. Shinoe T, Matsui M, Taketo MM, Manabe T, (2005) Modulation of synaptic plasticity by physiological activation of M-1 muscarinic acetylcholine receptors in the mouse hippocampus. Journal of Neuroscience 25: 11194-11200.
2. Anagnostaras SG, Murphy GG, Hamilton SE, Mitchell SL, Rahnama NP, et al. (2003) Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice. Nat Neurosci 6: 51-58.
3. Wess J, (2004) Muscarinic acetylcholine receptor knockout mice: novel phenotypes and clinical implications. Annu Rev Pharmacol Toxicol 44: 423-450.
4. Seol GH, Ziburkus J, Huang S, Song L, Kim IT, et al. (2007) Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron 55: 919-929.
5. Boddeke EW, Enz A, Shapiro G, (1992) SDZ ENS 163, a selective muscarinic M1 receptor agonist, facilitates the induction of long-term potentiation in rat hippocampal slices. Eur J Pharmacol 222: 21-25.
6. Buchanan KA, Petrovic MM, Chamberlain SE, Marrion NV, Mellor JR, (2010) Facilitation of long-term potentiation by muscarinic M(1) receptors is mediated by inhibition of SK channels. Neuron 68: 948-963.
7. Dean B, Bymaster FP, Scarr E, (2003) Muscarinic receptors in schizophrenia. Curr Mol Med 3: 419-426.
8. Marino MJ, Rouse ST, Levey AI, Potter LT, Conn PJ, (1998) Activation of the genetically defined m1 muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proceedings of the National Academy of Sciences of the United States of America 95: 11465-11470.
9. Aramakis VB, Bandrowski AE, Ashe JH, (1999) Role of muscarinic receptors, G-proteins, and intracellular messengers in muscarinic modulation of NMDA receptor-mediated synaptic transmission. Synapse 32: 262-275.
10. Harvey J, Balasubramaniam R, Collingridge GL, (1993) Carbachol can potentiate N-methyl-D-aspartate responses in the rat hippocampus by a staurosporine and thapsigargin-insensitive mechanism. Neurosci Lett 162: 165-168.
11. Markram H, Segal M, (1992) The inositol 1,4,5-trisphosphate pathway mediates cholinergic potentiation of rat hippocampal neuronal responses to NMDA. J Physiol 447: 513-533.
12. Giessel AJ, Sabatini BL, (2010) M1 muscarinic receptors boost synaptic potentials and calcium influx in dendritic spines by inhibiting postsynaptic SK channels. Neuron 68: 936-947.
13. Madison DV, Lancaster B, Nicoll RA, (1987) Voltage Clamp Analysis of Cholinergic Action in the Hippocampus. Journal of Neuroscience 7: 733-741.
14. Marrion NV, Smart TG, Marsh SJ, Brown DA, (1989) Muscarinic suppression of the M-current in the rat sympathetic ganglion is mediated by receptors of the M1-subtype. Br J Pharmacol 98: 557-573.
15. Brown DA, Adams PR, (1980) Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283: 673-676.
16. Suh BC, Hille B, (2002) Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron 35: 507-520.
17. Suh BC, Inoue T, Meyer T, Hille B, (2006) Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels. Science 314: 1454-1457.
18. Li Y, Gamper N, Hilgemann DW, Shapiro MS, (2005) Regulation of Kv7 (KCNQ) K+ channel open probability by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25: 9825-9835.
19. Zhang H, Craciun LC, Mirshahi T, Rohacs T, Lopes CM, et al. (2003) PIP(2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 37: 963-975.
20. Gu N, Hu H, Vervaeke K, Storm JF, (2008) SK (KCa2) channels do not control somatic excitability in CA1 pyramidal neurons but can be activated by dendritic excitatory synapses and regulate their impact. J Neurophysiol 100: 2589-2604.
21. Behnisch T, Reymann KG, (1998) Inhibition of apamin-sensitive calcium dependent potassium channels facilitate the induction of long-term potentiation in the CA1 region of rat hippocampus in vitro. Neurosci Lett 253: 91-94.
22. Faber ES, Delaney AJ, Sah P, (2005) SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nat Neurosci 8: 635-641.
23. Ngo-Anh TJ, Bloodgood BL, Lin M, Sabatini BL, Maylie J, et al. (2005) SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines. Nat Neurosci 8: 642-649.
24. Bloodgood BL, Sabatini BL, (2007) Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron 53: 249-260.
25. Faber ES, (2010) Functional interplay between NMDA receptors, SK channels and voltage-gated Ca2+ channels regulates synaptic excitability in the medial prefrontal cortex. J Physiol 588: 1281-1292.
26. Yue C, Yaari Y, (2004) KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J Neurosci 24: 4614-4624.
27. Gu N, Vervaeke K, Hu H, Storm JF, (2005) Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566: 689-715.
28. Brown JT, Randall AD, (2009) Activity-dependent depression of the spike after-depolarization generates long-lasting intrinsic plasticity in hippocampal CA3 pyramidal neurons. J Physiol 587: 1265-1281.
29. Fontan-Lozano A, Suarez-Pereira I, Delgado-Garcia JM, Carrion AM, (2011) The M-current inhibitor XE991 decreases the stimulation threshold for long-term synaptic plasticity in healthy mice and in models of cognitive disease. Hippocampus 21: 22-32.
30. Song MK, Cui YY, Zhang WW, Zhu L, Lu Y, et al. (2009) The facilitating effect of systemic administration of Kv7/M channel blocker XE991 on LTP induction in the hippocampal CA1 area independent of muscarinic activation. Neurosci Lett 461: 25-29.
31. Lampe BJ, Gaskill JL, Keim SC, Brown BS, (1997) Linopirdine reduces stimulus intensity threshold for induction of long-term potentiation in the Schaffer collateral/CA1 pathway in rat hippocampal slices. Neurosci Lett 222: 135-137.
32. Tsubokawa H, Ross WN, (1997) Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons. Journal of Neuroscience 17: 5782-5791.
33. Robinson HP, (2008) A scriptable DSP-based system for dynamic conductance injection. J Neurosci Methods 169: 271-281.
34. Hodgkin AL, Huxley AF, (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500-544.
35. Nowacki J, Osinga HM, Brown JT, Randall AD, Tsaneva-Atanasova K, (2011) A unified model of CA1/3 pyramidal cells: an investigation into excitability. Prog Biophys Mol Biol 105: 34-48.
36. Soldovieri MV, Cilio MR, Miceli F, Bellini G, Miraglia del Giudice E, et al. (2007) Atypical gating of M-type potassium channels conferred by mutations in uncharged residues in the S4 region of KCNQ2 causing benign familial neonatal convulsions. J Neurosci 27: 4919-4928.
37. Oldfield S, Hancock J, Mason A, Hobson SA, Wynick D, et al. (2009) Receptor-mediated suppression of potassium currents requires colocalization within lipid rafts. Mol Pharmacol 76: 1279-1289.
38. Buchanan KA, Mellor JR, (2007) The development of synaptic plasticity induction rules and the requirement for postsynaptic spikes in rat hippocampal CA1 pyramidal neurones. Journal of Physiology 585: 429-445.
39. Shah MM, Migliore M, Valencia I, Cooper EC, Brown DA, (2008) Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 105: 7869-7874.
40. Hu H, Vervaeke K, Storm JF, (2007) M-channels (Kv7/KCNQ channels) that regulate synaptic integration, excitability, and spike pattern of CA1 pyramidal cells are located in the perisomatic region. J Neurosci 27: 1853-1867.
41. Brown JT, Booth CA, Randall AD, (2011) Synaptic activation of mGluR1 generates persistent depression of a fast after-depolarizing potential in CA3 pyramidal neurons. Eur J Neurosci 33: 879-889.
42. Martire M, Castaldo P, D'Amico M, Preziosi P, Annunziato L, et al. (2004) M channels containing KCNQ2 subunits modulate norepinephrine, aspartate, and GABA release from hippocampal nerve terminals. J Neurosci 24: 592-597.
43. Peretz A, Sheinin A, Yue C, Degani-Katzav N, Gibor G, et al. (2007) Pre- and postsynaptic activation of M-channels by a novel opener dampens neuronal firing and transmitter release. J Neurophysiol 97: 283-295.
44. Prinz AA, Abbott LF, Marder E, (2004) The dynamic clamp comes of age. Trends Neurosci 27: 218-224.
45. Ma M, Koester J, (1996) The role of K+ currents in frequency-dependent spike broadening in Aplysia R20 neurons: a dynamic-clamp analysis. J Neurosci 16: 4089-4101.
46. Destexhe A, Bal T, (2009) Dynamic-Clamp: From Principles to Applications New York Springer.
47. Tzingounis AV, Heidenreich M, Kharkovets T, Spitzmaul G, Jensen HS, et al. (2010) The KCNQ5 potassium channel mediates a component of the afterhyperpolarization current in mouse hippocampus. Proc Natl Acad Sci U S A 107: 10232-10237.
48. Tzingounis AV, Nicoll RA, (2008) Contribution of KCNQ2 and KCNQ3 to the medium and slow afterhyperpolarization currents. Proc Natl Acad Sci U S A 105: 19974-19979.
49. Yamasaki M, Matsui M, Watanabe M, (2010) Preferential localization of muscarinic M1 receptor on dendritic shaft and spine of cortical pyramidal cells and its anatomical evidence for volume transmission. J Neurosci 30: 4408-4418.
50. Levey AI, Edmunds SM, Koliatsos V, Wiley RG, Heilman CJ, (1995) Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci 15: 4077-4092.
51. Wu WW, Chan CS, Surmeier DJ, Disterhoft JF, (2008) Coupling of L-type Ca2+ channels to KV7/KCNQ channels creates a novel, activity-dependent, homeostatic intrinsic plasticity. J Neurophysiol 100: 1897-1908.
52. Schroeder BC, Hechenberger M, Weinreich F, Kubisch C, Jentsch TJ, (2000) KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. J Biol Chem 275: 24089-24095.
53. Singh NA, Charlier C, Stauffer D, DuPont BR, Leach RJ, et al. (1998) A novel potassium channel gene, KCNQ2, is mutated in an inherited epilepsy of newborns. Nat Genet 18: 25-29.
54. Charlier C, Singh NA, Ryan SG, Lewis TB, Reus BE, et al. (1998) A pore mutation in a novel KQT-like potassium channel gene in an idiopathic epilepsy family. Nat Genet 18: 53-55.
55. Peters HC, Hu H, Pongs O, Storm JF, Isbrandt D, (2005) Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat Neurosci 8: 51-60.
56. Oh MM, Kuo AG, Wu WW, Sametsky EA, Disterhoft JF, (2003) Watermaze learning enhances excitability of CA1 pyramidal neurons. J Neurophysiol 90: 2171-2179.